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ATP and AMP Mutually Influence Their Interaction with the ATP-binding Cassette (ABC) Adenylate Kinase Cystic Fibrosis Transmembrane Conductance Regulator (CFTR) at Separate Binding Sites
Journal article   Open access   Peer reviewed

ATP and AMP Mutually Influence Their Interaction with the ATP-binding Cassette (ABC) Adenylate Kinase Cystic Fibrosis Transmembrane Conductance Regulator (CFTR) at Separate Binding Sites

Christoph O Randak, Qian Dong, Amanda R Ver Heul, Adrian H Elcock and Michael J Welsh
The Journal of biological chemistry, Vol.288(38), pp.27692-27701
09/20/2013
DOI: 10.1074/jbc.M113.479675
PMCID: PMC3779764
PMID: 23921386
url
https://doi.org/10.1074/jbc.M113.479675View
Published (Version of record) Open Access

Abstract

Background: Cystic fibrosis transmembrane conductance regulator (CFTR) has adenylate kinase activity (ATP + AMP ⇆ 2 ADP). Results: ATP enables CFTR photolabeling by 8-N 3 -AMP, and AMP increases 8-N 3 -ATP photolabeling at ATP-binding site 2. Conclusion: AMP interacts with CFTR in an ATP-dependent manner and alters ATP interaction with the adenylate kinase active center ATP-binding site. Significance: These findings exemplify nucleotide interactions with an ABC adenylate kinase. Cystic fibrosis transmembrane conductance regulator (CFTR) is an anion channel in the ATP-binding cassette (ABC) transporter protein family. In the presence of ATP and physiologically relevant concentrations of AMP, CFTR exhibits adenylate kinase activity (ATP + AMP ⇆ 2 ADP). Previous studies suggested that the interaction of nucleotide triphosphate with CFTR at ATP-binding site 2 is required for this activity. Two other ABC proteins, Rad50 and a structural maintenance of chromosome protein, also have adenylate kinase activity. All three ABC adenylate kinases bind and hydrolyze ATP in the absence of other nucleotides. However, little is known about how an ABC adenylate kinase interacts with ATP and AMP when both are present. Based on data from non-ABC adenylate kinases, we hypothesized that ATP and AMP mutually influence their interaction with CFTR at separate binding sites. We further hypothesized that only one of the two CFTR ATP-binding sites is involved in the adenylate kinase reaction. We found that 8-azidoadenosine 5′-triphosphate (8-N 3 -ATP) and 8-azidoadenosine 5′-monophosphate (8-N 3 -AMP) photolabeled separate sites in CFTR. Labeling of the AMP-binding site with 8-N 3 -AMP required the presence of ATP. Conversely, AMP enhanced photolabeling with 8-N 3 -ATP at ATP-binding site 2. The adenylate kinase active center probe P 1 ,P 5 -di(adenosine-5′) pentaphosphate interacted simultaneously with an AMP-binding site and ATP-binding site 2. These results show that ATP and AMP interact with separate binding sites but mutually influence their interaction with the ABC adenylate kinase CFTR. They further indicate that the active center of the adenylate kinase comprises ATP-binding site 2.
Genetic Diseases AMP ABC Transporter Cystic fibrosis Enzymology ATP CFTR

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